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      Glucose uptake to guard cells via STP transporters provides carbon sources for stomatal opening and plant growth

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          Abstract

          Guard cells on the leaf epidermis regulate stomatal opening for gas exchange between plants and the atmosphere, allowing a balance between photosynthesis and transpiration. Given that guard cells possess several characteristics of sink tissues, their metabolic activities should largely depend on mesophyll‐derived sugars. Early biochemical studies revealed sugar uptake into guard cells. However, the transporters that are involved and their relative contribution to guard cell function are not yet known. Here, we identified the monosaccharide/proton symporters Sugar Transport Protein 1 and 4 ( STP1 and STP4) as the major plasma membrane hexose sugar transporters in the guard cells of Arabidopsis thaliana. We show that their combined action is required for glucose import to guard cells, providing carbon sources for starch accumulation and light‐induced stomatal opening that are essential for plant growth. These findings highlight mesophyll‐derived glucose as an important metabolite connecting stomatal movements with photosynthesis.

          Abstract

          This study uncovers a new role for plasma membrane Sugar Transport Protein 1 and 4 ( STP1/ STP4) in glucose uptake to Arabidopsis thaliana guard cells, which is essential for stomatal movements and plant growth.

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          Most cited references63

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          Genome-wide insertional mutagenesis of Arabidopsis thaliana.

          J M Alonso (2003)
          Over 225,000 independent Agrobacterium transferred DNA (T-DNA) insertion events in the genome of the reference plant Arabidopsis thaliana have been created that represent near saturation of the gene space. The precise locations were determined for more than 88,000 T-DNA insertions, which resulted in the identification of mutations in more than 21,700 of the approximately 29,454 predicted Arabidopsis genes. Genome-wide analysis of the distribution of integration events revealed the existence of a large integration site bias at both the chromosome and gene levels. Insertion mutations were identified in genes that are regulated in response to the plant hormone ethylene.
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            Transport of sugars.

            Soluble sugars serve five main purposes in multicellular organisms: as sources of carbon skeletons, osmolytes, signals, and transient energy storage and as transport molecules. Most sugars are derived from photosynthetic organisms, particularly plants. In multicellular organisms, some cells specialize in providing sugars to other cells (e.g., intestinal and liver cells in animals, photosynthetic cells in plants), whereas others depend completely on an external supply (e.g., brain cells, roots and seeds). This cellular exchange of sugars requires transport proteins to mediate uptake or release from cells or subcellular compartments. Thus, not surprisingly, sugar transport is critical for plants, animals, and humans. At present, three classes of eukaryotic sugar transporters have been characterized, namely the glucose transporters (GLUTs), sodium-glucose symporters (SGLTs), and SWEETs. This review presents the history and state of the art of sugar transporter research, covering genetics, biochemistry, and physiology-from their identification and characterization to their structure, function, and physiology. In humans, understanding sugar transport has therapeutic importance (e.g., addressing diabetes or limiting access of cancer cells to sugars), and in plants, these transporters are critical for crop yield and pathogen susceptibility.
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              The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis.

              Stomata are pores on the leaf surface, bounded by two guard cells, which control the uptake of CO(2) for photosynthesis and the concomitant loss of water vapor. In 1898, Francis Darwin showed that stomata close in response to reduced atmospheric relative humidity (rh); however, our understanding of the signaling pathway responsible for coupling changes in rh to alterations in stomatal aperture is fragmentary. The results presented here highlight the primacy of abscisic acid (ABA) in the stomatal response to drying air. We show that guard cells possess the entire ABA biosynthesis pathway and that it appears upregulated by positive feedback by ABA. When wild-type Arabidopsis and the ABA-deficient mutant aba3-1 were exposed to reductions in rh, the aba3-1 mutant wilted, whereas the wild-type did not. However, when aba3-1 plants, in which ABA synthesis had been specifically rescued in guard cells, were challenged with dry air, they did not wilt. These data indicate that guard cell-autonomous ABA synthesis is required for and is sufficient for stomatal closure in response to low rh. Guard cell-autonomous ABA synthesis allows the plant to tailor leaf gas exchange exquisitely to suit the prevailing environmental conditions. Copyright © 2013 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                dsantelia@ethz.ch
                Journal
                EMBO Rep
                EMBO Rep
                10.1002/(ISSN)1469-3178
                EMBR
                embor
                EMBO Reports
                John Wiley and Sons Inc. (Hoboken )
                1469-221X
                1469-3178
                06 July 2020
                05 August 2020
                06 July 2020
                : 21
                : 8 ( doiID: 10.1002/embr.v21.8 )
                : e49719
                Affiliations
                [ 1 ] Institute of Integrative Biology ETH Zürich Zürich Switzerland
                [ 2 ] Department of Plant and Microbial Biology University of Zürich Zürich Switzerland
                [ 3 ] Photon Systems Instruments (PSI) Drasov Czech Republic
                [ 4 ]Present address: Syngenta Crop Protection AG Stein AG Switzerland
                [ 5 ]Present address: John Innes Centre Norwich Research Park Norwich UK
                Author notes
                [*] [* ]Corresponding author. Tel: +41 44 632 89 27; E‐mail: dsantelia@ 123456ethz.ch
                [†]

                These authors contributed equally to this work

                Author information
                https://orcid.org/0000-0001-7020-6520
                https://orcid.org/0000-0002-6260-1448
                https://orcid.org/0000-0001-9686-1216
                Article
                EMBR201949719
                10.15252/embr.201949719
                7403697
                32627357
                4f4339bf-cca0-455b-86fc-e260ca1399ca
                © 2020 The Authors. Published under the terms of the CC BY 4.0 license

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 20 November 2019
                : 08 May 2020
                : 13 May 2020
                Page count
                Figures: 9, Tables: 0, Pages: 13, Words: 12644
                Funding
                Funded by: European Union's Horizon 2020 , open-funder-registry 10.13039/501100007601;
                Award ID: PITN‐GA‐2013‐608422—IDP BRIDGES, 722338—PlantHUB
                Funded by: University of Zürich , open-funder-registry 10.13039/501100006447;
                Funded by: Swiss National Science Foundation , open-funder-registry 10.13039/501100001711;
                Award ID: 31003A_166539
                Award ID: 310030_185241
                Funded by: ETH Zürich , open-funder-registry 10.13039/501100003006;
                Categories
                Article
                Articles
                Custom metadata
                2.0
                05 August 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.6 mode:remove_FC converted:05.08.2020

                Molecular biology
                glucose,guard cells,plant growth,stomatal opening,sugar transport protein,metabolism,plant biology

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